John H. Ashe

Synaptic Potentials and Effects of Amino Acid Antagonists in the Auditory Cortex

Neurons of in vitro guinea pig and rat auditory cortex receive a complex synaptic pattern of afferent information. As many as four synaptic responses to a single-stimulus pulse to the gray or white matter can occur; an early-EPSP followed, sequentially, by an early-IPSP, late-EPSP, and late-IPSP. Paired pulse stimulation and pharmacological studies show that the early-IPSP can modify information transmission that occurs by way of the early-EPSP. Each of these four synaptic responses differed in estimated reversal potential, and each was differentially sensitive to antagonism by pharmacological agents. DNQX (6,7-dinitroquinoxaline-2,3-dione), a quisqualate/kainate receptor antagonist, blocked the early-EPSP, and the late-EPSP was blocked by the NMDA receptor antagonist APV (D-2-amino-5-phosphonovalerate). The early-IPSP was blocked by the GABA-a receptor antagonist bicuculline, and the late-IPSP by the GABA-b receptor antagonists 2-OH saclofen or phaclofen. Presentation of stimulus trains, even at relatively low intensities, could produce a long-lasting APV-sensitive membrane depolarization. Also discussed is the possible role of these synaptic potentials in auditory cortical function and plasticity.

Stimulus Characteristics in Food Aversion Learning

One of the more intriguing issues in contemporary learning theory is the idea that stimuli are not equally associable. This idea, that some associations are more easily formed than others, has been formulated in various ways using such concepts as belongingness (Thorndike, 1932; Rozin and Kalat, 1971), stimulus relevance (Capretta, 1961), cue to consequence (Garcia and Koelling, 1966), and preparedness (Seligman, 1970). In food aversion learning, it is clear that animals readily learn to avoid ingesting material which was associated with sickness. (We use the words illness or sickness as arbitrary convenient terms in this chapter, realizing full well that they represent a gross oversimplification. The nature of the UCS is an important problem deserving of more consideration than can be given in this chapter.) The early field studies on bait shyness added poisons to bait and it became evident that animals learned to avoid the specific bait (Chitty, 1954). In subsequent laboratory experiments, the use of solutions permitted the control of other stimulus factors and it was possible to demonstrate that it was primarily the taste rather than any other sensory quality that was avoided (Garcia, Kimeldorf, and Koelling, 1955; Nachman, 1963).

Sensory system neural activity during habituation of the pupillary orienting reflex

The possible role of sensory system evoked activity in the habituation of the orienting reflex was examined by recording simultaneously multiple unit activity and pupillary responses to repeated tactile and acoustic stimulation. Cats bearing electrodes chronically implanted in the somatosensory and auditory systems were tested during neuromuscular paralysis in order to ensure constancy of stimulus intensity at the receptors and permit precise monitoring of pupillary size. Tactile and acoustic stimulation produced evoked responses in both of these sensory systems. Both tactile stimulation (1/3 sec) and acoustic stimulation (1/min) resulted in habituation of the pupillary dilation component of the orienting reflex which was accompanied by decrements in somatosensory and auditory system evoked activity. The cochlear nucleus was unresponsive to tactile stimulation, and did not exhibit response decrements during acoustic stimulation. Background activity increased in the auditory cortex during tactile habituation, and in the somatic cortex during auditory habituation. The results indicate that systematic decrements in sensory evoked multiple unit activity could be of functional significance to the habituation of the orienting reflex and that specific effects upon sensory cortex do develop during behavioral habituation.

Acetylcholine Modulation of Cellular Excitability Via Muscarinic Receptors: Functional Plasticity in Auditory Cortex

In recent years substantial advancement has occurred toward understanding integrative functions of the nervous system. Acetylcholine (ACh), dopamine (DA), norepinephrine (NE), and serotonin (5-HT), are substances that have gained general recognition as neurotransmitters in the sense of having a direct influence on the magnitude of membrane potential. These substances are now also characterized as neuromodulators, a designation which encompasses observations of complex electrophysiologic and metabolic effects in target neurons that occur in addition to, or are independent of, simple excitatory and inhibitory changes in the membrane potential (for reviews, see Dismukes, 1979; Kupfermann, 1979; Daly et al., 1980; Kaczmarek and Levitan, 1987).

The relationship of the cochlear microphonic potential to the acquisition of a classically conditioned pupillary dilation response

The possible role of the peripheral auditory apparatus in the acquisition of a behavioral conditioned response was investigated by simultaneously recording the cochlear microphonic and the pupillary dilation response during Pavlovian conditioning procedures. Chronically prepared, paralyzed cats were used to insure acoustic stimulus constancy at the cochlea. Sensitization and differentiation procedures were employed to control for nonassociative factors. During conditioning, the pupillary dilation response systematically increased, in contrast to the cochlear microphonic response, which failed to exhibit either consistent increases or decreases. During discrimination training, the pupillary dilation response exhibited consistent differential responses to the acoustic CS+ and CS−, whereas the cochlear microphonic failed to do so. The present findings support the view that conditioning of auditory system multiple unit activity is not the result of systematic changes at the cochlea.

Multifiber efferent activity in postganglionic sympathetic and parasympathetic nerves related to the latency of spontaneous and evoked pupillary dilation.

Abstract Spontaneous and peripherally evoked multifiber potentials were recorded from the sympathetic and parasympathetic pupillomotor fibers of the acutely prepared, pharmacologically immobilized cat. The onset latency of change in axonal activity was compared to the onset latency of pupillary dilation of the contralateral iris. Spontaneous pupillary dilations were accompanied by inhibition of parasympathetic and excitation of sympathetic pupillomotor activity. However, parasympathetic inhibition precedes sympathetic excitation. As with spontaneous changes, evoked changes in parasympathetic discharge rate occurred with a shorter onset latency than changes in sympapathetic discharge. In addition, the onset latency of change in sympathetic and parasympathetic nerve discharge was not related to the onset latency of evoked pupillary dilation by a constant factor. The difference in latency of the neural and pupillary response was found to increase systematically as a function of the latency of pupillary dilation.

Mesencephalic Multiple-Unit Activity During Acquisition of Conditioned Pupillary Dilation

Multiple-unit recordings were obtained from the interstitial nucleus of Cajal, nucleus of Darkschewitsch and the superior colliculus of the cat during acquisition of classically conditioned pupillary dilation. Multiple-unit responses in all regions were enhanced by conditioning procedures. However, only the acquisition functions for the accessory oculomotor nuclei, i.e., interstitial nucleus of Cajal and nucleus of Darkschewitsch, were significantly correlated with the acquisition of conditioned pupillary dilation. These results were discussed in relation to the mechanism of autonomic control of conditioned pupillary dilation. It was concluded that inhibition of parasympathetic pupillomotor efferents via the accessory oculomotor nuclei may play a role in the acquisition of conditioned pupillary dilation.

Role of the parasympathetic pupillomotor system in classically conditioned pupillary dilation of the cat

The involvement of the parasympathetic pupillomotor system in the acquisition of conditioned pupillary dilation response was investigated by simultaneously recording the activity of the sympathectomized iris and the contralateral intact iris during Pavlovian conditioning procedures. Chronically prepared, pharmacologically immobilized cats were used to insure acoustic stimulus constancy at the cochlea. Sensitization procedures were employed to control for nonassociative factors. During conditioning, the pupillary dilation response of both the intact and the sympathectomized iris systematically increased with CS—UCS presentation. Despite the fact that the sympathectomized iris was tonically smaller than the intact iris, and that the dilations in the former were smaller than in the latter, the form of dilations and constrictions was nearly identical in the two eyes. During training, the sympathectomized iris exhibits dynamics identical to those of the intact eye. The most pronounced difference between the response of the pupils was that the asymptotic amplitude of the conditioned response is as great as that of the unconditioned response to shock for the sympathectomized iris, but not for the intact iris. The present findings support the view that acquisition of conditioned pupillary dilation response in the cat is primarily mediated by inhibition of parasympathetic activity. However, the actual contribution of the sympathetic pupillomotor system remains to be determined by parallel experiments using the parasympathectomized preparation.

Effects of stimulus omission during habituation of the pupillary dilation reflex

The pupillary dilation reflex of the paralyzed cat was studied during habituation to an acoustic stimulus. The effect of a scheduled stimulus omission was assessed by examination of pupillary activity during the omission, in the 4-sec intertrial interval, and on the following trial. It was found that dilation responses during the omission were rare. Effects were seen more often in the intertrial interval or on the following trial (“dishabituation”). Responses to an omitted stimulus were related to the dynamics of background (“tonic”) pupillary size; specifically, they occurred significantly more often for subjects which exhibited an increase in background pupillary diameter following initial stimuli and then a decrease during the later course of habituation.

Responses of opossum and rat hippocampal CA1 cells to paired stimulus volleys

Short-term synaptic plasticity was studied in the in vitro hippocampus of the North American opossum (Didelphis virginiana) and rat (Rattus norvegicus). Conditioning and test stimulus pulses were delivered to fibers in stratum radiatum, and intracellular and extracellular recordings were obtained from area CA1 pyramidal cells. In rat, the amplitude of the population spike in response to the second (test) of two stimulus impulses is suppressed at short inter-pulse-intervals (IPIs). In opossum, the amplitude of the test population spike is facilitated at comparable IPIs. Facilitation of the test population spike in rat occurs only when the test stimulus is separated from the first stimulus (conditioning) by a longer IPI. Peak values of facilitation do not significantly differ between species. Intracellular responses, elicited by stimulus pulses that were subthreshold for spike production, indicate that the amplitude of test EPSPs recorded from opossum pyramidal cells are facilitated at IPIs that result in suppression of test EPSPs in rat pyramidal cells.